Interpretive Summary: The microsporidian Nosema ceranae has recently invaded managed honey bee (Apis mellifera) colonies beyond Asia. The presence of this emergent parasite in lineages of A. mellifera that are naïve to its selection pressure (“Italian”) and that have co-evolved with the parasite over ca. 150 generations ("Russian") provided an opportunity to test the parasite hypothesis for the evolution of polyandry (i.e., multiple mating by queens). We investigated the relationship between infection levels of N. ceranae and sub-family (patriline) membership of honey bees by sampling individual worker bees from both Russian and Italian stocks. Differences among stocks and colonies of each stock were evident for both Russian and Italian honey bees. A relationship between patriline and nosema levels was only found in Russian honey bees. These results support the parasite hypothesis and are the first report of genetic variation in response to Nosema infection in honey bees.

Technical Abstract:
The microsporidian Nosema ceranae has recently invaded managed honey bee (Apis mellifera) colonies beyond Asia. The presence of this emergent parasite in lineages of A. mellifera that are naïve to its selection pressure (“Italian”) and that have co-evolved with the parasite over ca. 150 generations ("Russian") provided an opportunity to test the parasite hypothesis for the evolution of polyandry. We investigated the relationship between infection levels of N. ceranae and patriline membership by sampling individual worker bees from 5 colonies from each of the Russian and Italian lineages. Individual workers were tested for N. ceranae infection level using qPCR of the LSU rDNA, and then genotyped to determine their patriline membership. Levels of N. ceranae infestation differed significantly between lineages (Russian: 4 x 106 ± 1.9 x 106 Nosema/bee and Italian: 9 x 106 ± 5 x 106 Nosema/bee; P < 0.0001) and colonies for both Russian (P < 0.0001) and Italian (P < 0.0001) workers. Patriline-based variance was evident only among the Russian workers (P = 0.02). There was substantial variation in N. ceranae levels among Italian workers, ranging from 0 to 2 x 109 Nosema /bee, but this variation was unrelated to patriline membership (P = 0.67). These results are congruent with predictions derived from the parasite hypothesis for the evolution of polyandry – patrilinial variance in parasite tolerance contributes to colony-level resistance by reducing the probability of catastrophic failure that might occur if a colony were genetically homogeneous.